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PMID: 22517320 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Fern and lycophyte guard cells do not respond to endogenous abscisic acid.

The Plant cell ·Vol. 24 ·No. 4 ·2012-04-00 ·Pages 1510-21

McAdam SA, Brodribb TJ

Abstract

Stomatal guard cells regulate plant photosynthesis and transpiration. Central to the control of seed plant stomatal movement is the phytohormone abscisic acid (ABA); however, differences in the sensitivity of guard cells to this ubiquitous chemical have been reported across land plant lineages. Using a phylogenetic approach to investigate guard cell control, we examined the diversity of stomatal responses to endogenous ABA and leaf water potential during water stress. We show that although all species respond similarly to leaf water deficit in terms of enhanced levels of ABA and closed stomata, the function of fern and lycophyte stomata diverged strongly from seed plant species upon rehydration. When instantaneously rehydrated from a water-stressed state, fern and lycophyte stomata rapidly reopened to predrought levels despite the high levels of endogenous ABA in the leaf. In seed plants under the same conditions, high levels of ABA in the leaf prevented rapid reopening of stomata. We conclude that endogenous ABA synthesized by ferns and lycophytes plays little role in the regulation of transpiration, with stomata passively responsive to leaf water potential. These results support a gradualistic model of stomatal control evolution, offering opportunities for molecular and guard cell biochemical studies to gain further insights into stomatal control.

MeSH Terms
Abscisic Acid/pharmacology Dehydration Droughts Ferns/cytology,drug effects,physiology Plant Stomata/cytology,drug effects,physiology Plant Transpiration/drug effects,physiology Selaginellaceae/cytology,drug effects,physiology Species Specificity Water
Chemicals
Water Abscisic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
McAdam Scott A M
School of Plant Science, University of Tasmania, Hobart, Tasmania 7001, Australia.
Brodribb Timothy J
References (52)
52 references, click to expand
  1. Are diurnal patterns of stomatal movement the result of alternating metabolism of endogenous guard cell ABA and accumulation of ABA delivered to the apoplast around guard cells by transpiration?
    J Exp Bot. 2004 Sep;55(405):1963-76 PMID: 15310824
  2. The protein kinase SnRK2.6 mediates the regulation of sucrose metabolism and plant growth in Arabidopsis.
    Plant Physiol. 2010 May;153(1):99-113 PMID: 20200070
  3. The identification of genes involved in the stomatal response to reduced atmospheric relative humidity.
    Curr Biol. 2006 May 9;16(9):882-7 PMID: 16682349
  4. Opinion: stomatal responses to light and CO(2) depend on the mesophyll.
    Plant Cell Environ. 2009 Nov;32(11):1479-86 PMID: 19627565
  5. ABA-based chemical signalling: the co-ordination of responses to stress in plants.
    Plant Cell Environ. 2002 Feb;25(2):195-210 PMID: 11841663
  6. OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells.
    Trends Plant Sci. 2003 Apr;8(4):151-3 PMID: 12711225
  7. An overview of models of stomatal conductance at the leaf level.
    Plant Cell Environ. 2010 Sep;33(9):1419-38 PMID: 20545879
  8. Abscisic Acid Accumulation by in Situ and Isolated Guard Cells of Pisum sativum L. and Vicia faba L. in Relation to Water Stress.
    Plant Physiol. 1986 Aug;81(4):1017-21 PMID: 16664936
  9. ABA in bryophytes: how a universal growth regulator in life became a plant hormone?
    J Plant Res. 2011 Jul;124(4):437-53 PMID: 21416316
  10. Occurrence, function and potential medicinal applications of the phytohormone abscisic acid in animals and humans.
    Biochem Pharmacol. 2011 Oct 1;82(7):701-12 PMID: 21763293
  11. Major transitions in the evolution of early land plants: a bryological perspective.
    Ann Bot. 2012 Apr;109(5):851-71 PMID: 22356739
  12. Phenotypic reversion of flacca, a wilty mutant of tomato, by abscisic Acid.
    Science. 1970 Aug 7;169(3945):592-3 PMID: 17746034
  13. A new, vapour-phase mechanism for stomatal responses to humidity and temperature.
    Plant Cell Environ. 2011 Jan;34(1):162-78 PMID: 20880202
  14. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling.
    Annu Rev Plant Biol. 2010;61:561-91 PMID: 20192751
  15. The control of stomata by water balance.
    New Phytol. 2005 Nov;168(2):275-92 PMID: 16219068
  16. Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum.
    New Phytol. 2009;183(4):1053-1063 PMID: 19552695
  17. Stomatal response to abscisic Acid is a function of current plant water status.
    Plant Physiol. 1992 Feb;98(2):540-5 PMID: 16668674
  18. Passive origins of stomatal control in vascular plants.
    Science. 2011 Feb 4;331(6017):582-5 PMID: 21163966
  19. Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis.
    Plant Physiol. 2005 Jan;137(1):209-19 PMID: 15618419
  20. Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution.
    Curr Biol. 2011 Jun 21;21(12):1025-9 PMID: 21658944
  21. Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism.
    Plant Cell Environ. 2009 Aug;32(8):949-59 PMID: 19302171
  22. Evolution of stomatal responsiveness to CO(2) and optimization of water-use efficiency among land plants.
    New Phytol. 2009 Aug;183(3):839-847 PMID: 19402882
  23. Transpiration and assimilation of early Devonian land plants with axially symmetric telomes-simulations on the tissue level.
    J Theor Biol. 2000 Sep 7;206(1):91-107 PMID: 10968940
  24. Stomatal innovation and the rise of seed plants.
    Ecol Lett. 2012 Jan;15(1):1-8 PMID: 22017636
  25. Origin and evolution of genes related to ABA metabolism and its signaling pathways.
    J Plant Res. 2011 Jul;124(4):455-65 PMID: 21626211
  26. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants.
    Plant Cell. 1997 Mar;9(3):409-23 PMID: 9090884
  27. Guard cell photosynthesis and stomatal function.
    New Phytol. 2009;181(1):13-34 PMID: 19076715
  28. Abscisic acid signaling in seeds and seedlings.
    Plant Cell. 2002;14 Suppl:S15-45 PMID: 12045268
  29. Hydraulic failure defines the recovery and point of death in water-stressed conifers.
    Plant Physiol. 2009 Jan;149(1):575-84 PMID: 19011001
  30. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.
    Nature. 2000 Aug 17;406(6797):731-4 PMID: 10963598
  31. The fern Adiantum capillus-veneris lacks stomatal responses to blue light.
    Plant Cell Physiol. 2006 Jun;47(6):748-55 PMID: 16621842
  32. Augmentation of abscisic acid (ABA) levels by drought does not induce short-term stomatal sensitivity to CO2 in two divergent conifer species.
    J Exp Bot. 2011 Jan;62(1):195-203 PMID: 20797996
  33. ABA signal transduction at the crossroad of biotic and abiotic stress responses.
    Plant Cell Environ. 2012 Jan;35(1):53-60 PMID: 21923759
  34. GUARD CELL SIGNAL TRANSDUCTION.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:627-658 PMID: 11337411
  35. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy.
    Plant Cell Physiol. 2009 Jul;50(7):1345-63 PMID: 19541597
  36. Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system.
    Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6472-7 PMID: 17395720
  37. Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements.
    Plant J. 2010 Jun 1;62(6):1072-82 PMID: 20345603
  38. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1.
    Sci Signal. 2011 May 17;4(173):ra32 PMID: 21586729
  39. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities.
    Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):8023-8 PMID: 20385816
  40. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.
    Curr Opin Plant Biol. 2000 Jun;3(3):217-23 PMID: 10837265
  41. Land plants acquired active stomatal control early in their evolutionary history.
    Curr Biol. 2011 Jun 21;21(12):1030-5 PMID: 21658945
  42. Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo.
    Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1717-22 PMID: 21220313
  43. The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells.
    Plant Physiol. 2008 Jun;147(2):922-30 PMID: 18467462
  44. Stomatal control as a driver of plant evolution.
    J Exp Bot. 2011 May;62(8):2419-23 PMID: 21576397
  45. An abscisic acid-related reduced transpiration promotes gradual embolism repair when grapevines are rehydrated after drought.
    New Phytol. 2008;180(3):642-651 PMID: 18700860
  46. The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells.
    Plant Cell. 2009 Jul;21(7):2143-62 PMID: 19638476
  47. Inactivation of AtRac1 by abscisic acid is essential for stomatal closure.
    Genes Dev. 2001 Jul 15;15(14):1808-16 PMID: 11459830
  48. Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling.
    PLoS Biol. 2006 Oct;4(10):e312 PMID: 16968132
  49. Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses.
    Ann Bot. 2012 Jan;109(1):5-17 PMID: 21994053
  50. ABA- and cADPR-mediated effects on respiration and filtration downstream of the temperature-signaling cascade in sponges.
    J Cell Sci. 2003 Feb 15;116(Pt 4):629-36 PMID: 12538763
  51. CO(2) signaling in guard cells: calcium sensitivity response modulation, a Ca(2+)-independent phase, and CO(2) insensitivity of the gca2 mutant.
    Proc Natl Acad Sci U S A. 2006 May 9;103(19):7506-11 PMID: 16651523
  52. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production.
    Plant Cell. 2002 Dec;14(12):3089-99 PMID: 12468729
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2012-04-00
Epub
2012-00-18
Pages
1510-21
Language
English
Region
England
NLM ID
9208688
PMCID
PMC3398560
Subset
IM
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